Research Article| Volume 102, 105871, February 2023

American Society of Biomechanics Clinical Biomechanics Award 2021: Redistribution of muscle-tendon work in children with cerebral palsy who walk in crouch


      • Characterized Achilles and patellar tendon loading with shear wave tensiometry.
      • Triceps surae exhibits spring-like behavior in crouch gait due to cerebral palsy.
      • Quadriceps exhibit motor-like, positive work in crouch due to cerebral palsy.
      • Redistribution in work relevant for treatment planning to correct crouch.



      Previous study showed the triceps surae exhibits spring-like behavior about the ankle during walking in children with cerebral palsy. Thus, the work generated by the triceps surae is diminished relative to typically developing children. This study investigated whether the quadriceps offset the lack of triceps surae work production in children with cerebral palsy who walk in crouch.


      Seven children with cerebral palsy (8-16 yrs) and 14 typically developing controls (8-17 yrs) walked overground at their preferred speed in a motion analysis laboratory. Shear wave tensiometers were used to track patellar and Achilles tendon loading throughout the gait cycle. Tendon force measures were coupled with muscle-tendon kinematic estimates to characterize the net work generated by the quadriceps and triceps surae about the knee and ankle, respectively.


      Children with cerebral palsy generated significantly less triceps surae work when compared to controls (P < 0.001). The reverse was true at the knee. Children with cerebral palsy generated positive net work from the quadriceps about the knee, which exceeded the net quadriceps work generated by controls (P = 0.028).


      There was a marked difference in functional behavior of the triceps surae and quadriceps in children with cerebral palsy who walk in crouch. In particular, the triceps surae of children with cerebral palsy exhibited spring-like behavior about the ankle while the quadriceps exhibited more motor-like behavior about the knee. This redistribution in work could partly be associated with the elevated energetic cost of walking in children with cerebral palsy and is relevant to consider when planning treatments to correct crouch gait.


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        • Alexander C.F.
        • Reid S.
        • Stannage K.
        • Dwyer B.
        • Elliott C.
        • Valentine J.
        • Donnelly C.J.
        Children with cerebral palsy have larger Achilles tendon moment arms than typically developing children.
        J. Biomech. 2019; 82: 307-312
        • Barber L.
        • Barrett R.
        • Lichtwark G.
        Medial gastrocnemius muscle fascicle active torque-length and Achilles tendon properties in young adults with spastic cerebral palsy.
        J. Biomech. 2012; 45: 2526-2530
        • Biewener A.A.
        • McGowan C.
        • Card G.M.
        • Baudinette R.V.
        Dynamics of leg muscle function in tammar wallabies (M. eugenii) during level versus incline hopping.
        J. Exp. Biol. 2004; 207: 211-223
        • Bohannon R.W.
        • Smith M.B.
        Interrater reliability of a modified Ashworth scale of muscle spasticity.
        Phys. Ther. 1987;
        • Cespedes I.
        Methods for estimation of subsample time delays of digitized echo signals.
        Ultrason. Imaging. 1995; 17: 142-171
        • Cheewasukanon S.
        • Osateerakun P.
        • Limpaphayom N.
        Recurrence of knee flexion contracture after surgical correction in children with cerebral palsy.
        Int. Orthop. 2021; 45: 1523-1530
        • Dickinson M.H.
        • Farley C.T.
        • Full R.J.
        • Koehl M.A.R.
        • Kram R.
        • Lehamn S.
        How animals move: an integrative view.
        Science (80-. ). 2000; 288: 100-106
        • Dietz F.R.
        • Albright J.C.
        • Dolan L.
        Medium-term follow-up of Achilles tendon lengthening in the treatment of ankle equinus in cerebral palsy.
        Iowa Orthop. J. 2006; 26: 27-32
        • Ebrahimi A.
        • Loegering I.F.
        • Martin J.A.
        • Pomeroy R.L.
        • Roth J.D.
        • Thelen D.G.
        Achilles tendon loading is lower in older adults than young adults across a broad range of walking speeds.
        Exp. Gerontol. 2020; 137110966
        • Ebrahimi A.
        • Martin J.A.
        • Schmitz D.G.
        • Thelen D.G.
        Shear wave tensiometry reveals an age-related deficit in triceps surae work at slow and fast walking speeds.
        Front. Sport. Act. Living. 2020; 2
        • Ebrahimi A.
        • Kuchler R.L.
        • Pomeroy R.L.
        • Loegering I.F.
        • Martin J.A.
        • Thelen D.G.
        Normative Achilles and patellar tendon shear wave speeds and loading patterns during walking in typically developing children.
        Gait Posture. 2021; 88: 185-191
        • Ebrahimi A.
        • Schwartz M.H.
        • Martin J.A.
        • Novacheck T.F.
        • Thelen D.G.
        Atypical triceps surae force and work patterns underlying gait in children with cerebral palsy.
        J. Orthop. Res. 2022; : 1-8
        • Frigo C.
        • Crenna P.
        • Jensen L.M.
        Moment-angle relationship at lower limb joints during human walking at different velocities.
        J. Electromyogr. Kinesiol. 1996; 6: 177-190
        • Gage J.R.
        • Novacheck T.F.
        An update on the treatment of gait problems in cerebral palsy.
        J. Pediatr. Orthop. B. 2001; 10: 265-274
      1. Gage J.R. Schwartz M.H. Koop S.E. Novacheck T.F. The Identification and Treatment of Gait Problems in Cerebral Palsy. 2nd ed. Mac Keith Press, London2009
        • Galey S.A.
        • Lerner Z.F.
        • Bulea T.C.
        • Zimbler S.
        • Damiano D.L.
        Effectiveness of surgical and non-surgical management of crouch gait in cerebral palsy: a systematic review.
        Gait Posture. 2017; 54: 93-105
        • Hermens H.J.
        • Freriks B.
        • Merletti R.
        • Stegeman D.
        • Blok J.
        • Rau G.
        • Disselhorst-Klug C.
        • Hägg G.
        European recommendations for surface ElectroMyoGraphy.
        Roessingh Res. Dev. 1999; : 8-11
        • Huang T.W.P.
        • Shorter K.A.
        • Adamczyk P.G.
        • Kuo A.D.
        Mechanical and energetic consequences of reduced ankle plantar-flexion in human walking.
        J. Exp. Biol. 2015; 218: 3541-3550
        • Josephson R.K.
        Mechanical power output from striated muscle during cyclic contraction.
        J. Exp. Biol. 1985; 114: 493-512
        • Kalkman B.M.
        • Bar-On L.
        • Cenni F.
        • Maganaris C.N.
        • Bass A.
        • Holmes G.
        • Desloovere K.
        • Barton G.J.
        • O’Brien T.D.
        Achilles tendon moment arm length is smaller in children with cerebral palsy than in typically developing children.
        J. Biomech. 2017; 56: 48-54
        • Kautz S.A.
        • Brown D.A.
        Relationships between timing of muscle excitation and impaired motor performance during cyclical lower extremity movement in post-stroke hemiplegia.
        Brain. 1998; 121: 515-526
        • Keuler E.
        • Loegering I.
        • Martin J.
        • Roth J.
        • Thelen D.
        Shear wave predictions of achilles tendon loading during human walking.
        Sci. Rep. 2019; : 1-9
        • Kuo A.D.
        Energetics of actively powered locomotion using the simplest walking model.
        J. Biomech. Eng. 2002; 124: 113-120
        • Martin J.A.
        • Brandon S.C.E.
        • Keuler E.M.
        • Hermus J.R.
        • Ehlers A.C.
        • Segalman D.J.
        • Allen M.S.
        • Thelen D.G.
        Gauging force by tapping tendons.
        Nat. Commun. 2018; 9: 1-9
        • Martin J.A.
        • Schmitz D.G.
        • Ehlers A.C.
        • Allen M.S.
        • Thelen D.G.
        Calibration of the shear wave speed-stress relationship in ex vivo tendons.
        J. Biomech. 2019; 90: 9-15
        • Martin J.A.
        • Kindig M.W.
        • Stender C.J.
        • Ledoux W.R.
        • Thelen D.G.
        Calibration of the shear wave speed-stress relationship in in situ Achilles tendons using cadaveric simulations of gait and isometric contraction.
        J. Biomech. 2020; 106109799
        • Mathewson M.A.
        • Lieber R.L.
        Pathophysiology of muscle contractures in cerebral palsy.
        Phys. Med. Rehabil. Clin. N. Am. 2015; 26: 57-67
        • Perry J.
        Gait Analysis: Normal and Pathological Function.
        Thorofare, NJ1992
        • Rose J.
        • McGill K.C.
        Neuromuscular activation and motor-unit firing characteristics in cerebral palsy.
        Dev. Med. Child Neurol. 2005; 47: 329-336
        • Rose J.
        • Haskell W.L.
        • Gamble J.G.
        • Hamilton R.L.
        • Brown D.A.
        • Rinsky L.
        Muscle pathology and clinical measures of disability in children with cerebral palsy.
        J. Orthop. Res. 1994; 12: 758-768
        • Sala D.A.
        • Grant A.D.
        • Kummer F.J.
        Equinus deformity in cerebral palsy: recurrence after tendo Achillis lengthening.
        Dev. Med. Child Neurol. 2008; 39: 45-48
        • Sawicki G.S.
        • Robertson B.D.
        • Azizi E.
        • Roberts T.J.
        Timing matters: tuning the mechanics of a muscle-tendon unit by adjusting stimulation phase during cyclic contractions.
        J. Exp. Biol. 2015; 218: 3150-3159
        • Schwartz M.H.
        • Rozumalski A.
        • Trost J.P.
        The effect of walking speed on the gait of typically developing children.
        J. Biomech. 2008; 41: 1639-1650
        • Schwartz M.H.
        • Rozumalski A.
        • Steele K.M.
        Dynamic motor control is associated with treatment outcomes for children with cerebral palsy.
        Dev. Med. Child Neurol. 2016; 58: 1139-1145
        • Shore B.J.
        • White N.
        • Graham H.K.
        Surgical correction of equinus deformity in children with cerebral palsy: a systematic review.
        J. Child. Orthop. 2010; 4: 277-290
        • Sorsdahl A.B.
        • Moe-Nilssen R.
        • Strand L.I.
        Test–retest reliability of spatial and temporal gait parameters in children with cerebral palsy as measured by an electronic walkway.
        Gait Posture. 2008; 27: 43-50
        • Steele K.M.
        • Rozumalski A.
        • Schwartz M.H.
        Muscle synergies and complexity of neuromuscular control during gait in cerebral palsy.
        Dev. Med. Child Neurol. 2015; 57: 1176-1182
        • Steele K.M.
        • Shuman B.R.
        • Schwartz M.H.
        Crouch severity is a poor predictor of elevated oxygen consumption in cerebral palsy.
        J. Biomech. 2017; 60: 170-174
        • Theis N.
        • Mohagheghi A.A.
        • Korff T.
        Mechanical and material properties of the plantarflexor muscles and Achilles tendon in children with spastic cerebral palsy and typically developing children.
        J. Biomech. 2016; 49: 3004-3008
        • Waters R.L.
        • Mulroy S.
        The energy expenditure of normal and pathologic gait.
        Gait Posture. 1999; 9: 207-231
        • Wren T.A.L.
        • Rethlefsen S.
        • Kay R.M.
        Prevalence of specific gait abnormalities in children with cerebral palsy.
        J. Pediatr. Orthop. 2005; 25: 79-83
        • Wren T.A.L.
        • Cheatwood A.P.
        • Rethlefsen S.A.
        • Hara R.
        • Perez F.J.
        • Kay R.M.
        Achilles tendon length and medial gastrocnemius architecture in children with cerebral palsy and equinus gait.
        J. Pediatr. Orthop. 2010; 30: 479-484
        • Wutzke C.J.
        • Sawicki G.S.
        • Lewek M.D.
        The influence of a unilateral fixed ankle on metabolic and mechanical demands during walking in unimpaired young adults.
        J. Biomech. 2012; 45: 2405-2410